Influence of low-level prenatal exposure to PCDD/Fs and PCBs on empathizing, systemizing and autistic traits: Results from the duisburg birth cohort study

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Nowack, Nikola ^a   Wittsiepe, Jürgen ^a   Kasper Sonnenberg, Monika ^a   Wilhelm, Michael ^a   Schölmerich, Axel ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ENDOCRINE DISRUPTOR; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN; TESTOSTERONE; BENZOFURAN DERIVATIVE; POLLUTANT;

ADULT; ARTICLE; AUTISM; AUTISM ASSESSMENT; BLOOD SAMPLING; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; EMPATHY; FEMALE; HUMAN; MALE; MATERNAL BLOOD; PREGNANCY; PRENATAL EXPOSURE; RATING SCALE; SOCIAL RESPONSIVENESS SCALE; ADVERSE EFFECTS; ANALOGS AND DERIVATIVES; AUTISM SPECTRUM DISORDER; BLOOD; GERMANY; POLLUTANT;

ADULT; AUTISM SPECTRUM DISORDER; BENZOFURANS; CHILD; DIBENZOFURANS, POLYCHLORINATED; ENVIRONMENTAL POLLUTANTS; FEMALE; GERMANY; HUMANS; MALE; POLYCHLORINATED BIPHENYLS; POLYCHLORINATED DIBENZODIOXINS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84935457999     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0129906     Document Type: Article

References (119)

1. American Psychiatric Association. DSM IV Diagnostic and statistical manual of mental disorders. 4th ed. Washington, DC: American Psychiatric Association; 1994.
2. Baron-Cohen S. The extreme male brain theory of autism. Trends Cogn Sci. 2002 Jun 1; 6: 248-254. PMID: 12039606
3. Baron-Cohen S, Scott FJ, Allison C, Williams J, Bolton P, Matthews FE, et al. Prevalence of autismspectrum conditions: UK school-based population study. Br J Psychiatry. 2009 Jun; 194: 500-509. doi: 10.1192/bjp.bp.108.059345 PMID: 19478287
4. Center for Disease Control and Prevention (2014) Autism Spectrum Disorder (ASD) Data & Statistics. Available: http://www.cdc.gov/ncbddd/autism/data.html.
5. Sutcliffe JS. Insights into the Pathogenesis of Autism. Science. 2008; 321: 208-209. doi: 10.1126/ science.1160555 PMID: 18621658
6. Hertz-Picciotto I, Delwiche L. The rise in autism and the role of age at diagnosis. Epidemiology. 2009; 20: 84-90. doi: 10.1097/EDE.0b013e3181902d15 PMID: 19234401
7. Becerra TA, Wilhelm M, Olsen J, Cockburn M, Ritz B. Ambient Air Pollution and Autism in Los Angeles County, California. Environ Health Perspect. 2013 Mar; 121: 380-386. doi: 10.1289/ehp.1205827 PMID: 23249813
8. Kalkbrenner AE, Daniels JL, Chen J, Poole C, Emch M, Morrissey J. Perinatal Exposure to Hazardous Air Pollutants and Autism Spectrum Disorders at Age 8. Epidemiology. 2010 Sep; 21: 631-641. doi: 10.1097/EDE.0b013e3181e65d76 PMID: 20562626
9. Roberts AL, Lyall K, Hart JE, Laden F, Just AC, Bobb JF, et al. Perinatal Air Pollutant Exposures and Autism Spectrum Disorder in the Children of Nurses' Health Study II Participants. Environ Health Perspect. 2013 Aug; 121: 978-984. doi: 10.1289/ehp.1206187 PMID: 23816781
10. Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R. Residential Proximity to Freeways and Autism in the CHARGE Study. Environ Health Perspect. 2011 Jun; 119: 873-877. doi: 10.1289/ ehp.1002835 PMID: 21156395
11. Volk HE, Lurmann F, Penfold B, Hertz-Picciotto I, McConnell R. Traffic-Related Air Pollution, Particulate Matter, and Autism. JAMA Psychiatry. 2013 Jan; 70: 71-77. doi: 10.1001/jamapsychiatry.2013. 266 PMID: 23404082
12. Windham GC, Zhang L, Gunier R, Croen LA, Grether JK. Autism Spectrum Disorders in Relation to Distribution of Hazardous Air Pollutants in the San Francisco Bay Area. Environ Health Perspect. 2006 Sep; 114: 1438-1444. PMID: 16966102
13. Larsson M, Weiss B, Janson S, Sundell J, Bornehag C. Associations between indoor environmental factors and parental-reported autistic spectrum disorders in children 6-8 years of age. Neurotoxicology. 2009 Sep; 30: 822-831. doi: 10.1016/j.neuro.2009.01.011 PMID: 19822263
14. Miodovnik A, Engel SM, Zhu C, Ye X, Soorya LV, Silva MJ, et al. Endocrine disruptors and childhood social impairment. Neurotoxicology. 2011 Mar; 32: 261-267. doi: 10.1016/j.neuro.2010.12.009 PMID: 21182865
15. Roberts EM, English PB, Grether JK, Windham GC, Somberg L, Wolff C. Maternal Residence Near Agricultural Pesticide Applications and Autism Spectrum Disorders Among Children in the California Central Valley. Environ Health Perspect. 2007 Oct; 115: 1482-1489. PMID: 17938740
16. Kajta M, Wójtowicz A, Maćkowiak M, Lasoń W. Aryl hydrocarbon receptor-mediated apoptosis of neuronal cells: A possible interaction with estrogen receptor signaling. Neuroscience. 2009 Jan 23; 158: 811-822. doi: 10.1016/j.neuroscience.2008.10.045 PMID: 19027052
17. van den Berg M, Birnbaum LS, Denison M, de Vito M, Farland W, Feeley M, et al. The 2005 World Health Organization reevaluation of human and Mammalian toxic equivalency factors for dioxins and dioxin-like compounds. Toxicol Sci. 2006 Oct; 93: 223-241. PMID: 16829543
18. Al-Salman F, Plant N. Non-coplanar polychlorinated biphenyls (PCBs) are direct agonists for the human pregnane-X receptor and constitutive androstane receptor, and activate target gene expression in a tissue-specific manner. Toxicol Appl Pharmacol. 2012 Aug 15; 263: 7-13. doi: 10.1016/j. taap.2012.05.016 PMID: 22664347
19. Zoeller RT, Brown TR, Doan LL, Gore AC, Skakkebaek NE, Soto AM, et al. Endocrine-disrupting chemicals and public health protection: a statement of principles from The Endocrine Society. Endocrinology. 2012 Sep; 153: 4097-4110. doi: 10.1210/en.2012-1422 PMID: 22733974
20. Brouwer A, Longnecker MP, Birnbaum LS, Cogliano J, Kostyniak P, Moore J, et al. Characterization of potential endocrine-related health effects at low-dose levels of exposure to PCBs. Environ Health Perspect. 1999; 107 Suppl. 4: 639-649. PMID: 10421775
21. Winneke G, Walkowiak J, Lilienthal H. PCB-induced neurodevelopmental toxicity in human infants and its potential mediation by endocrine dysfunction. Toxicology. 2002; 181-182: 161-165.
22. Myers J, Guillette L, Swan S, vom Saal F. Endocrine Disruptor Chemicals: Overview. In: Jorgensen SE, Fath BD, editors. Encyclopedia of Ecology. 1st ed. Oxford: Elsevier; 2008. pp. 1265-1269.
23. Landrigan PJ. Pesticides and Polychlorinated Biphenyls (PCBs): An Analysis of the Evidence That They Impair Children's Neurobehavioral Development. Mol Genet Metab. 2001 May; 73: 11-17. PMID: 11350178
24. Kim SM, Han DH, Lyoo HS, Min KJ, Kim KH, Renshaw P. Exposure to Environmental Toxins in Mothers of Children with Autism Spectrum Disorder. Psychiatry Investig. 2010 Jun; 7: 122-127. doi: 10. 4306/pi.2010.7.2.122 PMID: 20577621
25. Cheslack-Postava K, Rantakokko PV, Hinkka-Yli-Salomäki S, Surcel H, McKeague IW, Kiviranta HA, et al. Maternal serum persistent organic pollutants in the Finnish Prenatal Study of Autism: A pilot study. Neurotoxicol Teratol. 2013; 38: 1-5. doi: 10.1016/j.ntt.2013.04.001 PMID: 23591055
26. Mitchell MM, Woods R, Chi L, Schmidt RJ, Pessah IN, Kostyniak PJ, et al. Levels of select PCB and PBDE congeners in human postmortem brain reveal possible environmental involvement in 15q11-q13 duplication autism spectrum disorder. Environ Mol Mutagen. 2012 Oct; 53: 589-598. doi: 10. 1002/em.21722 PMID: 22930557
27. Otake T, Yoshinaga J, Seki Y, Matsumura T, Watanabe K, Ishijima M, et al. Retrospective in utero exposure assessment of PCBs using preserved umbilical cords and its application to case-control comparison. Environ Health Prev Med. 2006 Mar; 11: 65-68. doi: 10.1007/BF02898144 PMID: 21432364
28. Braun JM, Kalkbrenner AE, Just AC, Yolton K, Calafat AM, Sjödin A, et al. Gestational Exposure to Endocrine-Disrupting Chemicals and Reciprocal Social, Repetitive, and Stereotypic Behaviors in 4-and 5-Year-Old Children: The HOME Study. Environ Health Perspect. 2014 May; 122: 513-520. doi: 10.1289/ehp.1307261 PMID: 24622245
29. Nishijo M, Pham TT, Nguyen AT, Tran NN, Nakagawa H, Hoang LV, et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin in breast milk increases autistic traits of 3-year-old children in Vietnam. Mol Psychiatry. 2014; 19: 1220-1226. doi: 10.1038/mp.2014.18 PMID: 24637425
30. Nakagami A, Koyama T, Kawasaki K, Negishi T, Ihara T, Kuroda Y, et al. Maternal plasma polychlorinated biphenyl levels in cynomolgus monkeys (Macaca fascicularis) affect infant social skills in mother-infant interaction. Dev Psychobiol. 2011 Jan; 53: 79-88. doi: 10.1002/dev.20493 PMID: 20945409
31. Negishi T, Shimomura H, Koyama T, Kawasaki K, Ishii Y, Kyuwa S, et al. Gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin affects social behaviors between developing rhesus monkeys (Macaca mulatta). Toxicol Lett. 2006 Jan 25; 160: 233-244. PMID: 16125884
32. Kalkbrenner AE, Schmidt RJ, Penlesky AC. Environmental Chemical Exposures and Autism Spectrum Disorders: A Review of the Epidemiological Evidence. Curr Probl Pediatr Adolesc Health Care. 2014 Nov; 44: 1-42. doi: 10.1016/j.cppeds.2013.10.008 PMID: 24439025
33. Stein SA, Adams PM, Shanklin DR, Mihailoff GA, Palnitkar MB. Thyroid hormone control of brain and motor development: molecular, neuroanatomical, and behavioral studies. Adv Exp Med Biol. 1991; 299: 47-105. PMID: 1725685
34. Hagmar L. Polychlorinated biphenyls and thyroid status in humans: a review. Thyroid. 2003 Nov; 13: 1021-1028. PMID: 14651786
35. Breedlove S. Sexual dimorphism in the vertebrate nervous system. J Neurosci. 1992 Nov; 12: 4133-4142. PMID: 1432094
36. Gorski RA. Sexual dimorphisms of the brain. J Anim Sci. 1985; 61 Suppl. 3: 38-61. PMID: 3908433
37. Lenz KM, Nugent BM, McCarthy MM. Sexual Differentiation of the Rodent Brain: Dogma and Beyond. Front Neurosci. 2012 Feb 21; 6: 1-13. doi: 10.3389/fnins.2012.00001 PMID: 22294978
38. Morris JA, Jordan CL, Breedlove SM. Sexual differentiation of the vertebrate nervous system. Nat Neurosci. 2004 Oct; 7: 1034-1039. PMID: 15452574
39. Hines M, Davis FC, Coquelin A, Goy RW, Gorski RA. Sexually dimorphic regions in the medial preoptic area and the bed nucleus of the stria terminalis of the guinea pig brain: a description and an investigation of their relationship to gonadal steroids in adulthood. J Neurosci. 1985 Jan; 5: 40-47. PMID: 3965644
40. Jacobson CD, Csernus VJ, Shryne JE, Gorski RA. The influence of gonadectomy, androgen exposure, or a gonadal graft in the neonatal rat on the volume of the sexually dimorphic nucleus of the preoptic area. J Neurosci. 1981 Oct; 1: 1142-1147. PMID: 7288477
41. Morris JA, Jordan CL, Dugger BN, Breedlove SM. Partial demasculinization of several brain regions in adult male (XY) rats with a dysfunctional androgen receptor gene. J Comp Neurol. 2005 Jun 27; 487: 217-226. PMID: 15880473
42. Wallen K. Nature needs nurture: the interaction of hormonal and social influences on the development of behavioral sex differences in rhesus monkeys. Horm Behav. 1996 Dec; 30: 364-378. PMID: 9047263
43. Wu MV, Shah NM. Control of masculinization of the brain and behavior. Curr Opin Neurobiol. 2011 Feb; 21: 116-123. doi: 10.1016/j.conb.2010.09.014 PMID: 20970320
44. Baron-Cohen S, Knickmeyer RC, Belmonte MK. Sex differences in the brain: implications for explaining autism. Science. 2005 Nov 4; 310: 819-823. PMID: 16272115
45. Cohen-Bendahan CC, van de Beek C, Berenbaum SA. Prenatal sex hormone effects on child and adult sex-typed behavior: methods and findings. Neurosci Biobehav Rev. 2005 Apr; 29: 353-384. PMID: 15811504
46. Hampson E. Spatial cognition in humans: possible modulation by androgens and estrogens. J Psychiatry Neurosci. 1995 Nov; 20: 397-404. PMID: 8527425
47. Kimura D. Sex, sexual orientation and sex hormones influence human cognitive function. Curr Opin Neurobiol. 1996 Apr; 6: 259-263. PMID: 8725969
48. Vreugdenhil HJ, Slijper FM, Mulder PG, Weisglas-Kuperus N. Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age. Environ Health Perspect. 2002 Oct; 110: 593-598.
49. Winneke G, Ranft U, Wittsiepe J, Kasper-Sonnenberg M, Fürst P, Krämer U, et al. Behavioral Sexual Dimorphism in School-Age Children and Early Developmental Exposure to Dioxins and PCBs: A Follow-Up Study of the Duisburg Cohort. Environ Health Perspect. 2014 Mar; 122: 292-298. doi: 10. 1289/ehp.1306533 PMID: 24273228
50. Faass O, Ceccatelli R, Schlumpf M, Lichtensteiger W. Developmental effects of perinatal exposure to PBDE and PCB on gene expression in sexually dimorphic rat brain regions and female sexual behavior. Gen Comp Endocrinol. 2013; 188: 232-241. doi: 10.1016/j.ygcen.2013.04.008 PMID: 23619185
51. Chung Y, Nunez AA, Clemens LG. Effects of neonatal polychlorinated biphenyl exposure on female sexual behavior. Physiol Behav. 2001 Oct; 74: 363-370. PMID: 11714501
52. Wang XQ, Fang J, Nunez AA, Clemens LG. Developmental exposure to polychlorinated biphenyls affects sexual behavior of rats. Physiol Behav. 2002 Apr 15; 75: 689-696. PMID: 12020734
53. Meeker JD, Hauser R. Exposure to Polychlorinated Biphenyls (PCBs) and Male Reproduction. Syst Biol Reprod Med. 2010 Apr; 56: 122-131. doi: 10.3109/19396360903443658 PMID: 20377311
54. Goncharov A, Rej R, Negoita S, Schymura M, Santiago-Rivera A, Morse G, Carpenter DO. Lower serum testosterone associated with elevated polychlorinated biphenyl concentrations in Native American men. Environ Health Perspect. 2009 Sep; 117: 1454-1460. doi: 10.1289/ehp.0800134 PMID: 19750113
55. Cao Y, Winneke G, Wilhelm M, Wittsiepe J, Lemm F, Fürst P, et al. Environmental exposure to dioxins and polychlorinated biphenyls reduce levels of gonadal hormones in newborns: Results from the Duisburg cohort study. Int J Hyg Environ Health. 2008 Mar; 211: 30-39. PMID: 17660003
56. Knickmeyer RC, Baron-Cohen S. Topical Review: Fetal Testosterone and Sex Differences in Typical Social Development and in Autism. J Child Neurol. 2006 Oct; 21: 825-845. PMID: 17005117
57. Asperger H. Die .,Autistischen Psychopathen" im Kindesalter. Arch Psychiatr Nervenkr. 1944 Jun 3; 117: 76-136.
58. Auyeung B, Wheelwright S, Allison C, Atkinson M, Samarawickrema N, Baron-Cohen S. The Children's Empathy Quotient and Systemizing Quotient: Sex Differences in Typical Development and in Autism Spectrum Conditions. J Autism Dev Disord. 2009 Nov; 39: 1509-1521. doi: 10.1007/s10803-009-0772-x PMID: 19533317
59. Baron-Cohen S, Richler J, Bisarya D, Gurunathan N, Wheelwright S. The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. Philos Trans R Soc Lond B Biol Sci. 2003 Feb 28; 358: 361-374. PMID: 12639333
60. Baron-Cohen S, Wheelwright S. The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord. 2004 Apr; 34: 163-175. PMID: 15162935
61. Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G. Fetal testosterone and autistic traits. Br J Psychol. 2009 Feb; 100: 1-22. doi: 10.1348/000712608X311731 PMID: 18547459
62. Auyeung B, Taylor K, Hackett G, Baron-Cohen S. Foetal testosterone and autistic traits in 18 to 24-month-old children. Mol Autism. 2010 Jul 12; 1: 11. doi: 10.1186/2040-2392-1-11 PMID: 20678186
63. Baron-Cohen S, Auyeung B, Nørgaard-Pedersen B, Hougaard DM, Abdallah MW, Melgaard L, et al. Elevated fetal steroidogenic activity in autism. Mol Psychiatry. 2014 Jun 3. doi: 10.1038/mp.2014.48
64. Manning JT, Baron-Cohen S, Wheelwright S, Sanders G. The 2nd to 4th digit ratio and autism. Dev Med Child Neurol. 2001 Mar; 43: 160-164. PMID: 11263685
65. Wittsiepe J, Schrey P, Ewers U, Selenka F, Wilhelm M. Decrease of PCDD/F levels in human blood from Germany over the past ten years (1989-1998). Chemosphere. 2000 May-Jun; 40: 1103-1109. PMID: 10739052
66. Wilhelm M, Wittsiepe J, Lemm F, Ranft U, Krämer U, Fürst P, et al. The Duisburg birth cohort study: Influence of the prenatal exposure to PCDD/Fs and dioxin-like PCBs on thyroid hormone status in newborns and neurodevelopment of infants until the age of 24 months. Mutat Res Rev Mutat Res. 2008 Jul-Aug; 659: 83-92.
67. Rennert A, Wittsiepe J, Kasper-Sonnenberg M, Binder G, Fürst P, Cramer C, et al. Prenatal and Early Life Exposure to Polychlorinated Dibenzo-p-Dioxins, Dibenzofurans and Biphenyls May Influence Dehydroepiandrosterone Sulfate Levels at Prepubertal Age: Results from the Duisburg Birth Cohort Study. J Toxicol Environ Health A. 2012; 75: 1232-1240. doi: 10.1080/15287394.2012.709375 PMID: 22994577
68. Neugebauer J, Wittsiepe J, Kasper-Sonnenberg M, Schöneck N, Schölmerich A, Wilhelm M. The influence of low level pre- and perinatal exposure to PCDD/Fs, PCBs, and lead on attention performance and attention-related behavior among German school-aged children: Results from the Duisburg Birth Cohort Study. Int J Hyg Environ Health. 2014; 218: 153-162. doi: 10.1016/j.ijheh. 2014.09.005 PMID: 25456149
69. Schölmerich A. Empathy/Systemizing Quotient (EQ-SQ) (Child)-Deutsch. 2011. Available: www. autismresearchcentre.com/arc-tests.
70. Constantino JN. The Social Responsiveness Scale. Los Angeles, CA: Western Psychological Services; 2002.
71. Constantino JN, Gruber CP. Social Responsiveness Scale (SRS). Los Angeles, CA: Western Psychological Services; 2005.
72. Bölte S, Poustka F. Skala zur Erfassung sozialer Reaktivität (SRS). Bern: Huber; 2008.
73. Wittsiepe J, Fürst P, Schrey P, Lemm F, Kraft M, Eberwein G, et al. PCDD/F and dioxin-like PCB in human blood and milk from German mothers. Chemosphere. 2007 Apr; 67: 286-294.
74. Bölte S, Poustka F, Constantino JN. Assessing autistic traits: cross-cultural validation of the social responsiveness scale (SRS). Autism Res. 2008 Dec; 1: 354-363. doi: 10.1002/aur.49 PMID: 19360690
75. Bölte S, Westerwald E, Holtmann M, Freitag C, Poustka F. Autistic Traits and Autism Spectrum Disorders: The Clinical Validity of Two Measures Presuming a Continuum of Social Communication Skills. J Autism Dev Disord. 2011 Jan; 41: 66-72. doi: 10.1007/s10803-010-1024-9 PMID: 20422277
76. Charman T, Baird G, Simonoff E, Loucas T, Chandler S, Meldrum D, Pickles A. Efficacy of three screening instruments in the identification of autistic-spectrum disorders. Br J Psychiatry. 2007 Dec; 191: 554-559. PMID: 18055961
77. Constantino JN, Davis SA, Todd RD, Schindler MK, Gross MM, Brophy SL, et al. Validation of a brief quantitative measure of autistic traits: comparison of the social responsiveness scale with the autism diagnostic interview-revised. J Autism Dev Disord. 2003 Aug; 33: 427-433. PMID: 12959421
78. Murray MJ, Mayes SD, Smith LA. Brief Report: Excellent Agreement Between Two Brief Autism Scales (Checklist for Autism Spectrum Disorder and Social Responsiveness Scale) Completed Independently by Parents and the Autism Diagnostic Interview-Revised. J Autism Dev Disord. 2011 Nov; 41: 1586-1590. doi: 10.1007/s10803-011-1178-0 PMID: 21301946
79. Constantino JN, Lavesser PD, Zhang Y, Abbacchi AM, Gray T, Todd RD. Rapid quantitative assessment of autistic social impairment by classroom teachers. J Am Acad Child Adolesc Psychiatry. 2007 Dec; 46: 1668-1676. PMID: 18030089
80. Tewes U, Neubauer A, von Alster M. Wechsler Intelligenztest für Erwachsene (WIE). Bern: Huber; 2006.
81. Schantz SL, Ferguson SA, Bowman RE. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on behavior of monkeys in peer groups. Neurotoxicol Teratol. 1992 Nov-Dec; 14: 433-446. PMID: 1488038
82. Lutchmaya S, Baron-Cohen S, Raggatt P. Foetal testosterone and eye contact in 12-month-old human infants. Infant Behav Dev. 2002; 25: 327-335. doi: 10.1016/S0163-6383(02)00094-2
83. Lutchmaya S, Baron-Cohen S, Raggatt P. Foetal testosterone and vocabulary size in 18- and 24-month-old infants. Infant Behav Dev. 2001 Apr 18; 24: 418-424.
84. Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K, Hackett G. Fetal testosterone and empathy. Horm Behav. 2006 Mar; 49: 282-292. PMID: 16226265
85. Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K. Foetal testosterone, social relationships, and restricted interests in children. J Child Psychol & Psychiat. 2005 Feb; 46: 198-210.
86. Chapman E, Baron-Cohen S, Auyeung B, Knickmeyer R, Taylor K, Hackett G. Fetal testosterone and empathy: Evidence from the Empathy Quotient (EQ) and the "Reading the Mind in the Eyes" Test. Soc Neurosci. 2006; 1: 135-148. doi: 10.1080/17470910600992239 PMID: 18633782
87. Auyeung B, Baron-Cohen S, Chapman E, Knickmeyer R, Taylor K, Hackett G. Foetal testosterone and the child systemizing quotient. Eur J Endocrinol. 2006 Nov 1; 155: 123-130.
88. Auyeung B, Baron-Cohen S, Ashwin E, Knickmeyer R, Taylor K, Hackett G, et al. Fetal testosterone predicts sexually differentiated childhood behavior in girls and in boys. Psychol Sci. 2009 Feb; 20: 144-148. doi: 10.1111/j.1467-9280.2009.02279.x PMID: 19175758
89. Auyeung B, Knickmeyer R, Ashwin E, Taylor K, Hackett G, Baron-Cohen S. Effects of Fetal Testosterone on Visuospatial Ability. Arch Sex Behav. 2012 Jun; 41: 571-581. doi: 10.1007/s10508-011-9864-8 PMID: 22033667
90. Bonefeld-Jørgensen EC, Andersen HR, Rasmussen TH, Vinggaard AM. Effect of highly bioaccumulated polychlorinated biphenyl congeners on estrogen and androgen receptor activity. Toxicology. 2001 Feb 14; 158: 141-153. PMID: 11275356
91. Portigal CL, Cowell SP, Fedoruk MN, Butler CM, Rennie PS, Nelson CC. Polychlorinated biphenyls interfere with androgen-induced transcriptional activation and hormone binding. Toxicol Appl Pharmacol. 2002 Mar 15; 179: 185-194. PMID: 11906248
92. Chamberlain NL, Driver ED, Miesfeld RL. The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucleic Acids Res. 1994 Aug 11; 22: 3181-3186. PMID: 8065934
93. Manning JT, Bundred PE, Newton DJ, Flanagan BF. The second to fourth digit ratio and variation in the androgen receptor gene. Evol Hum Behav. 2003 Nov; 24: 399-405.
94. Colciago A, Negri-Cesi P, Pravettoni A, Mornati O, Casati L, Celotti F. Prenatal Aroclor 1254 exposure and brain sexual differentiation: Effect on the expression of testosterone metabolizing enzymes and androgen receptors in the hypothalamus of male and female rats. Reprod Toxicol. 2006 Nov; 22: 738-745. PMID: 16938428
95. Björk C, Lundberg Giwercman Y. Androgen receptor CAG repeat length modifies the effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on receptor activity in human prostate cells. Reprod Toxicol. 2013; 35: 144-149. doi: 10.1016/j.reprotox.2012.10.010 PMID: 23117151
96. Björk C, Nenonen H, Giwercman A, Bergman Å, Rylander L, Giwercman YL. Persistent organic pollutants have dose and CAG repeat length dependent effects on androgen receptor activity in vitro. Reprod Toxicol. 2011 Nov; 32: 293-297. doi: 10.1016/j.reprotox.2011.06.075 PMID: 21729750
97. Henningsson S, Jonsson L, Ljunggren E, Westberg L, Gillberg C, Råstam M, et al. Possible association between the androgen receptor gene and autism spectrum disorder. Psychoneuroendocrinology. 2009 Jun; 34: 752-761. doi: 10.1016/j.psyneuen.2008.12.007 PMID: 19167832
98. Kerdivel G, Habauzit D, Pakdel F. Assessment and Molecular Actions of Endocrine-Disrupting Chemicals That Interfere with Estrogen Receptor Pathways. Int J Endocrinol. 2013. doi: 10.1155/2013/ 501851
99. Kester MH, Bulduk S, Tibboel D, Meinl W, Glatt H, Falany CN, et al. Potent inhibition of estrogen sulfotransferase by hydroxylated PCB metabolites: a novel pathway explaining the estrogenic activity of PCBs. Endocrinology. 2000 May; 141: 1897-1900. PMID: 10803601
100. Kester MH, Bulduk S, van Toor H, Tibboel D, Meinl W, Glatt H, et al. Potent inhibition of estrogen sulfotransferase by hydroxylated metabolites of polyhalogenated aromatic hydrocarbons reveals alternative mechanism for estrogenic activity of endocrine disrupters. J Clin Endocrinol Metab. 2002 Mar; 87: 1142-1150. PMID: 11889178
101. Klinge CM, Kaur K, Swanson HI. The aryl hydrocarbon receptor interacts with estrogen receptor alpha and orphan receptors COUP-TFI and ERRalpha1. Arch Biochem Biophys. 2000 Jan; 373: 163-174. PMID: 10620335
102. Warner J, Osuch JR, Karmaus W, Landgraf JR, Taffe B, O'Keefe M, et al. Common classification schemes for PCB congeners and the gene expression of CYP17, CYP19, ESR1 and ESR2. Sci Total Environ. 2012; 414: 81-89. doi: 10.1016/j.scitotenv.2011.10.044 PMID: 22119029
103. Chakrabarti B, Dudbridge F, Kent L, Wheelwright S, Hill-Cawthorne G, Allison C, et al. Genes related to sex steroids, neural growth, and social-emotional behavior are associated with autistic traits, empathy, and Asperger syndrome. Autism Res. 2009 Jun; 2: 157-177. doi: 10.1002/aur.80 PMID: 19598235
104. Hedges VL, Ebner TJ, Meisel RL, Mermelstein PG. The cerebellum as a target for estrogen action. Front Neuroendocrinol. 2012 Oct; 33: 403-411. doi: 10.1016/j.yfrne.2012.08.005 PMID: 22975197
105. Fatemi SH, Aldinger KA, Ashwood P, Bauman ML, Blaha CD, Blatt GJ, et al. Consensus Paper: Pathological Role of the Cerebellum in Autism. Cerebellum. 2012 Sep; 11: 777-807. doi: 10.1007/ s12311-012-0355-9 PMID: 22370873
106. Kimura-Kuroda J, Nagata I, Kuroda Y. Disrupting effects of hydroxy-polychlorinated biphenyl (PCB) congeners on neuronal development of cerebellar Purkinje cells: A possible causal factor for developmental brain disorders? Chemosphere. 2007 Apr; 67: 412-420.
107. Hu VW. Is retinoic acid-related orphan receptor-alpha (RORA) a target for gene-environment interactions contributing to autism? Neurotoxicology. 2012 Dec; 33: 1434-1435. doi: 10.1016/j.neuro.2012. 07.009 PMID: 22967355
108. Hu VW, Sarachana T, Kim KS, Nguyen A, Kulkarni S, Steinberg ME, et al. Gene expression profiling differentiates autism case-controls and phenotypic variants of autism spectrum disorders: evidence for circadian rhythm dysfunction in severe autism. Autism Res. 2009 Apr; 2: 78-97. doi: 10.1002/aur. 73 PMID: 19418574
109. Nguyen A, Rauch TA, Pfeifer GP, Hu VW. Global methylation profiling of lymphoblastoid cell lines reveals epigenetic contributions to autism spectrum disorders and a novel autism candidate gene, RORA, whose protein product is reduced in autistic brain. FASEB J. 2010 Aug; 24: 3036-3051. doi: 10.1096/fj.10-154484 PMID: 20375269
110. Sarachana T, Hu VW. Genome-wide identification of transcriptional targets of RORA reveals direct regulation of multiple genes associated with autism spectrum disorder. Mol Autism. 2013 May 22; 4: 14. doi: 10.1186/2040-2392-4-14 PMID: 23697635
111. Sarachana T, Xu M, Wu R, Hu VW, Mattson M. Sex Hormones in Autism: Androgens and Estrogens Differentially and Reciprocally Regulate RORA, a Novel Candidate Gene for Autism. PLoS ONE. 2011 Feb 16. doi: 10.1371/journal.pone.0017116
112. Sarachana T, Hu VW. Differential recruitment of coregulators to the RORA promoter adds another layer of complexity to gene (dys) regulation by sex hormones in autism. Mol Autism. 2013 Oct 11; 4:39. doi: 10.1186/2040-2392-4-39 PMID: 24119295
113. Schantz S, Seo B, Moshtaghian J, Peterson R, Moore R. Effects of gestational and lactational exposure to TCDD or coplanar PCBs on spatial learning. Neurotoxicol Teratol. 1996 May-Jun; 18: 305-313. PMID: 8725643
114. Schantz S, Moshtaghian J, Ness D. Spatial Learning Deficits in Adult Rats Exposed to ortho-Substituted PCB Congeners during Gestation and Lactation. Fundam Appl Toxicol. 1995 Jun; 26: 117-126. PMID: 7657055
115. Berghuis SA, Soechitram SD, Hitzert MM, Sauer PJ, Bos AF. Prenatal exposure to polychlorinated biphenyls and their hydroxylated metabolites is associated with motor development of three-month-old infants. Neurotoxicology. 2013; 38: 124-130. doi: 10.1016/j.neuro.2013.07.003 PMID: 23895877
116. Roze E, Meijer L, Bakker A, van Braeckel KN, Sauer PJ, Bos AF. Prenatal Exposure to Organohalogens, Including Brominated Flame Retardants, Influences Motor, Cognitive, and Behavioral Performance at School Age. Environ Health Perspect. 2009 Dec; 117: 1953-1958. doi: 10.1289/ehp. 0901015 PMID: 20049217
117. Wright DB, Skagerberg EM. Measuring empathizing and systemizing with a large US sample. PLoS ONE. 2012. doi: 10.1371/journal.pone.0031661
118. Baron-Cohen S, Jolliffe T, Mortimore C, Robertson M. Another advanced test of theory of mind: evidence from very high functioning adults with autism or asperger syndrome. J Child Psychol Psychiatry. 1997 Oct; 38: 813-822. PMID: 9363580
119. Jolliffe T, Baron-Cohen S. Are people with autism and Asperger syndrome faster than normal on the Embedded Figures Test? J Child Psychol Psychiatry. 1997 Jul; 38: 527-534. PMID: 9255696